Deletion of the Transcriptional Regulator cyAbrB2 Deregulates Primary Carbon Metabolism in <i>Synechocystis</i> sp. PCC 6803

Kaniya, Yuki; Kizawa, Ayumi; Miyagi, Atsuko; Kawai‐Yamada, Maki; Uchimiya, Hirofumi; Kaneko, Yasuko; Nishiyama, Yoshikata; Hihara, Yukako

doi:10.1104/pp.113.218784

Cited by 44 publications

(37 citation statements)

References 29 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Ci metabolism in Synechocystis 6803 is controlled by three currently known transcriptional regulators: NdhR, CmpR, and CyAbrB2. CyAbrB2 appears to mediate between carbon and nitrogen regulation, because it controls gene transcription involved in both parts of metabolism (Ishii and Hihara, 2008;Lieman-Hurwitz et al, 2009;Yamauchi et al, 2011;Kaniya et al, 2013). In this study, CyAbrB2 transcripts are slightly responsive to the reduced LC supply but not significantly altered in D4.…”

Section: Deregulation Of CI Control In the D4 Mutantmentioning

confidence: 55%

See 1 more Smart Citation

Integrated analysis of engineered carbon limitation in a quadruple CO2/HCO3--uptake mutant of Synechocystis sp. PCC 6803

et al. 2015

View full text Add to dashboard Cite

ORCID IDs: 0000-0002-7224-9134 (I.O.); 0000-0002-2517-4440 (M.F.); 0000-0001-9675-4883 (J.K.).Cyanobacteria have efficient carbon concentration mechanisms and suppress photorespiration in response to inorganic carbon (Ci) limitation. We studied intracellular Ci limitation in the slow-growing CO 2 /HCO 3 2 -uptake mutant DndhD3 (for NADH dehydrogenase subunit D3)/ndhD4 (for NADH dehydrogenase subunit D4)/cmpA (for bicarbonate transport system substratebinding protein A)/sbtA (for sodium-dependent bicarbonate transporter A): D4 mutant of Synechocystis sp. PCC 6803. When cultivated under high-CO 2 conditions, Δ4 phenocopies wild-type metabolic and transcriptomic acclimation responses after the shift from high to low CO 2 supply. The Δ4 phenocopy reveals multiple compensation mechanisms and differs from the preacclimation of the transcriptional Ci regulator mutant ΔndhR (for ndhF3 operon transcriptional regulator). Contrary to the carboxysomeless ΔccmM (for carbon dioxide concentrating mechanism protein M) mutant, the metabolic photorespiratory burst triggered by shifting to low CO 2 is not enhanced in Δ4. However, levels of the photorespiratory intermediates 2-phosphoglycolate and glycine are increased under high CO 2 . The number of carboxysomes is increased in Δ4 under high-CO 2 conditions and appears to be the major contributing factor for the avoidance of photorespiration under intracellular Ci limitation. The Δ4 phenocopy is associated with the deregulation of Ci control, an overreduced cellular state, and limited photooxidative stress. Our data suggest multiple layers of Ci regulation, including inversely regulated modules of antisense RNAs and cognate target messenger RNAs and specific trans-acting small RNAs, such as the posttranscriptional PHOTOSYNTHESIS REGULATORY RNA1 (PsrR1), which shows increased expression in Δ4 and is involved in repressing many photosynthesis genes at the posttranscriptional level. In conclusion, our insights extend the knowledge on the range of compensatory responses of Synechocystis sp. PCC 6803 to intracellular Ci limitation and may become a valuable reference for improving biofuel production in cyanobacteria, in which Ci is channeled off from central metabolism and may thus become a limiting factor.Cyanobacteria evolved more than 2.5 billion years ago and shaped the atmosphere by decreasing the CO 2 concentration while increasing the proportion of molecular oxygen. In marine environments, cyanobacteria are still important CO 2 sinks and contribute significantly to the global carbon cycle (Stuart, 2011) via net fixation of inorganic carbon (Ci). Cyanobacteria are the evolutionary ancestors of all eukaryotic plastids (Mereschkowski, 1905;Deusch et al., 2008;Ochoa de Alda et al., 2014) and serve as prokaryotic models in which to study photosynthesis and plant Ci fixation.Rubisco catalyzes the central reaction of photosynthetic Ci fixation, in which ribulose-1,5-bisphosphate reacts with CO 2 to produce two molecules of 3-phosphoglycerate (3PGA). High levels of atmospheric CO 2 in Ea...

show abstract

Section: Deregulation Of CI Control In the D4 Mutantmentioning

confidence: 55%

“…Three transcriptional regulators of Ci utilization are known, CyAbrb2 (sll0822), CmpR (sll0030), and NdhR (also known as CcmR, sll1594). CyAbrb2 may balance carbon and nitrogen metabolism (Ishii and Hihara, 2008;LiemanHurwitz et al, 2009;Yamauchi et al, 2011;Kaniya et al, 2013). CmpR activates BCT1 expression under LC conditions (Omata et al, 2001).…”

mentioning

confidence: 99%

Integrated analysis of engineered carbon limitation in a quadruple CO2/HCO3--uptake mutant of Synechocystis sp. PCC 6803

et al. 2015

View full text Add to dashboard Cite

show abstract

“…Several AbrB-like transcriptional regulators (three in BL107 and two in WH8102) were induced in both strains at 18°C suggesting a potentially important role in low temperature acclimation ( Figure 5). In Synechocystis PCC6803, AbrB transcriptional regulators are known to have a role in carbon and nitrogen uptake and metabolism (Ishii and Hihara, 2008;Kaniya et al, 2013). These regulators may be involved in metabolic adjustments to low temperature.…”

Section: Molecular-level Adaptations To Growth Temperaturementioning

confidence: 99%

Effects of low temperature on tropical and temperate isolates of marine Synechococcus

et al. 2015

View full text Add to dashboard Cite

Temperature is an important factor influencing the distribution of marine picocyanobacteria. However, molecular responses contributing to temperature preferences are poorly understood in these important primary producers. We compared the temperature acclimation of a tropical Synechococcus strain WH8102 with temperate strain BL107 at 18°C relative to 22°C and examined their global protein expression, growth patterns, photosynthetic efficiency and lipid composition.Global protein expression profiles demonstrate the partitioning of the proteome into major categories: photosynthesis (440%), translation (10-15%) and membrane transport (2-8%) with distinct differences between and within strains grown at different temperatures. At low temperature, growth and photosynthesis of strain WH8102 was significantly decreased, while BL107 was largely unaffected. There was an increased abundance of proteins involved in protein biosynthesis at 18°C for BL107. Each strain showed distinct differences in lipid composition with higher unsaturation in strain BL107. We hypothesize that differences in membrane fluidity, abundance of protein biosynthesis machinery and the maintenance of photosynthesis efficiency contribute to the acclimation of strain BL107 to low temperature. Additional proteins unique to BL107 may also contribute to this strain's improved fitness at low temperature. Such adaptive capacities are likely important factors favoring growth of temperate strains over tropical strains in high latitude niches.

show abstract

“…PCC 6803 (hereafter, Synechocystis 6803): (1) the cyanobacterial homolog of the transition state regulator from Bacillus subtilis called cyAbrB2 (sll0822), (2) the regulator of the ATP-dependent bicarbonate transport system called CmpR (sll0030), and (3) NdhR (also called CcmR, CO 2 -concentrating mechanism regulator; sll1594). cyAbrB2 regulates the transcription of genes associated with both carbon and nitrogen metabolism (Ishii and Hihara, 2008;Lieman-Hurwitz et al, 2009;Kaniya et al, 2013). The regulator CmpR activates the expression of the cmpABCD operon encoding the high-affinity bicarbonate transporter called BCT1, which is induced under LC conditions (Omata et al, 2001).…”

mentioning

confidence: 99%

Integrated Transcriptomic and Metabolomic Characterization of the Low-Carbon Response Using an ndhR Mutant of Synechocystis sp. PCC 6803

et al. 2015

View full text Add to dashboard Cite

The acquisition and assimilation of inorganic carbon (Ci) represents the largest flux of inorganic matter in photosynthetic organisms; hence, this process is tightly regulated. We examined the Ci-dependent transcriptional and metabolic regulation in wild-type Synechocystis sp. PCC 6803 compared with a mutant defective in the main transcriptional repressor for Ci acquisition genes, the NAD(P)H dehydrogenase transcriptional regulator NdhR. The analysis revealed that many proteincoding transcripts that are normally repressed in the presence of high CO 2 (HC) concentrations were strongly expressed in ΔndhR, whereas other messenger RNAs were strongly down-regulated in mutant cells, suggesting a potential activating role for NdhR. A conserved NdhR-binding motif was identified in the promoters of derepressed genes. Interestingly, the expression of some NdhR-regulated genes remained further inducible under low-CO 2 conditions, indicating the involvement of additional NdhR-independent Ci-regulatory mechanisms. Intriguingly, we also observed that the abundance of 52 antisense RNAs and 34 potential noncoding RNAs was affected by Ci supply, although most of these molecules were not regulated through NdhR. Thus, antisense and noncoding RNAs could contribute to NdhR-independent carbon regulation. In contrast to the transcriptome, the metabolome in ΔndhR cells was similar to that of wild-type cells under HC conditions. This observation and the delayed metabolic responses to the low-CO 2 shift in ΔndhR, specifically the lack of transient increases in the photorespiratory pathway intermediates 2-phosphoglycolate, glycolate, and glycine, suggest that the deregulation of gene expression in the DndhR mutant successfully preacclimates cyanobacterial cells to lowered Ci supply under HC conditions. The acquisition and fixation of inorganic carbon (Ci) during photosynthesis generates an estimated net fixation of 210 gigatons of carbon per year (Stuart, 2011), representing the largest nutrient flux in living cells. Ci availability is often considered a limiting factor for photosynthetic performance. For example, in marine environments, the typical Ci level is constantly low at approximately 2 mM (Price et al., 2008). The central enzyme for photosynthetic carbon fixation is Rubisco, which catalyzes the carboxylation of ribulose-1, 5-bisphosphate (RubP), generating two molecules of 3-phosphoglycerate. As the evolutionary ancestors of all eukaryotic chloroplasts (Ochoa de Alda et al., 2014), cyanobacteria constitute the prokaryotic model for Ci acquisition. These organisms also represent a globally important CO 2 sink and are significant primary producers.The cyanobacterial Rubisco is adapted to the elevated CO 2 concentrations prevalent in the ancient atmosphere more than 350 million years ago (Berner, 1990). This apparent defect results in a rather low affinity for CO 2 compared with Rubisco in algae or land plants (Price et al., 2008). To ensure efficient carbon fixation in the present-day CO 2 -poor environment, cyanobacteria developed...

show abstract

Deletion of the Transcriptional Regulator cyAbrB2 Deregulates Primary Carbon Metabolism in Synechocystis sp. PCC 6803

Cited by 44 publications

References 29 publications

Integrated analysis of engineered carbon limitation in a quadruple CO2/HCO3--uptake mutant of Synechocystis sp. PCC 6803

Integrated analysis of engineered carbon limitation in a quadruple CO2/HCO3--uptake mutant of Synechocystis sp. PCC 6803

Effects of low temperature on tropical and temperate isolates of marine Synechococcus

Integrated Transcriptomic and Metabolomic Characterization of the Low-Carbon Response Using an ndhR Mutant of Synechocystis sp. PCC 6803

Contact Info

Product

Resources

About